Project area B "Genetics and Physiology" constitutes the natural bridge between investigation of Roseobacter clade bacteria in their full diversity and natural habitats down to the examination of the metabolic and regulatory principles of selected strains.
Here, the two selected model organisms Dinoroseobacter shibae and Phaeobacter gallaeciensis are investigated in connection with other thematically appropriate strains. Closely interconnected projects are analysing the energy metabolism and corresponding gene regulatory network of D. shibae with a broad spectrum of physiological, genetic and molecular biology methods.
Further, the pathways of secondary metabolite production with focus on antibiotic or signalling function are of central interest. Roseobacter clade-wide genome based searches and functional investigations will be combined with genetic and chemical studies using the two model systems D. shibae and P. gallaeciensis. Closely related are the questions for quorum sensing compounds and their biological function. The deduction of general principles for the versatile employment of metabolic strategies is envisaged.
B1 - Physiological response to energy limitation in the Roseobacter clade
B2 - Ecological significance of the secondary metabolite production by members of the Roseobacter clade
B3 - Biosynthetic pathways to secondary metabolites of the Roseobacter clade
B4 - Cell-cell-communication of bacteria of the Roseobacter clade with other bacteria and algae
B5 - Regulatory networks of the Dinoroseobacter shibae energy metabolism
B6 - Bacteriophages of the Roseobacter group
Physiological response to energy limitation in the Roseobacter clade
Ended
Principal investigator: Prof. Dr. Heribert Cypionka
PhD student: Christian Kirchhoff
Former PhD student: Maya Soora
Objectives and Projects
Dinoroseobacter shibae is an aerobic anoxygenic phototroph (AAP), capable of using light as an additional energy source under oxic conditions. While light is known to increase growth yields in continuous cultures only marginally, we suspected that the cells benefit from light particularly under conditions of carbon and electron donor limitation. Using Dinoroseobacter shibae as model organism we tested the hypothesis that the role of light energy for the cellular metabolism is proportional to the degree of starvation. We showed that light can indeed enhanced survival during long term starvation (Soora et al. 2013).
In a subsequent study we focused on cytotoxic reactive oxygen species which are produced as a direct result light exposure in D. shibae. We analyzed the role of the extrachromosomal elements (ECRs) and found that the genes of the oxygen stress response on the 72-kb chromid were strongly activated under light/dark cycle, compared to cells which grew in complete darkness. A Δ72-kb curing mutant lost the ability to survive under starvation in a light/dark cycle demonstrating the essential role of this chromid for oxidative stress adapation (Soora et al. 2015)
Tt was documented that light supports proton translocation and therefore contributes to the ATP regeneration in D. shibae (Holert et al. 2011). The mechanisms behind the fast recovery of the energy charge after anoxia are not clear yet. We addressed the bioenergetics of short-term anoxia and the quick ATP recovery in D. shibae. We hypothesized that the proton-motive force is involved, assuming that it would be low in de-energized cells and increase during recovery. Therefore we analyzed ΔpH and ΔΨ during oxic-anoxic transitions. We found that ΔpH is not affected by short-term anoxia and does not contribute to the quick ATP regeneration in D. shibae. By contrast, ΔΨ was increased during anoxia, which was astonishing since none of the control organisms behaved that way. For the lifestyle of D. shibae as an epibiont of a dinoflagellate, the ability to stand phases of temporary oxygen depletion is beneficial. With a boosted ΔΨ, the cells are able to give their ATP regeneration a flying start, once oxygen is available again. (Kirchhoff and Cypionka, submitted 2016).
Methods
Cultivation
Analysis of biomass-related parameters
Determination of physiological activities (schematics)
Activities
Publications:
Kirchhoff C, Ebert M, Jahn D, Cypionka H (2018) Chemiosmotic energy conservation in Dinoroseobacter shibae: Proton translocation driven by aerobic respiration, denitrification and photosynthetic light reaction. Front Microbiol doi:10.3389/fmicb.2018.00903.
Kirchhoff C, Cypionka H (2017) Propidium ion enters viable cells with high membrane potential during live-dead staining. J Microbiol Methods 142:79-82, https://doi.org/10.1016/j.mimet.2017.09.011.
Kirchhoff C, Cypionka H (2017) Boosted membrane potential as bioenergetic response to anoxia in Dinoroseobacter shibae. Front Microbiol, 8:695, https://doi.org/10.3389/fmicb.2017.00695.
Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, Wagner-Döbler I, Cypionka H (2015) Oxidative stress and starvation in Dinoroseobacter shibae: The role of extrachromosomal elements. Front Microbiol 6: 233, https://doi.org/10.3389/fmicb.2015.00233.
Soora M, Cypionka H (2013) Light enhances survival of Dinoroseobacter shibae during long-term starvation. PLoS ONE 8:e83960, https://doi.org/10.1371/journal.pone.0083960.
Holert J, Hahnke S, Cypionka H (2010) Influence of light and anoxia on chemiosmotic energy conservation in Dinoroseobacter shibae. Environm Microbiol Rep 3(1), 136-141, https://doi.org/10.1111/j.1758-2229.2010.00199.x.
Completed Master Thesis and Research Projects:
Christian Kirchhoff (Master Thesis) 2013. Key factors for the energy state of Dinoroseobacter shibae.
Robert Strodel (Reasearch Project) 2015. The sensitivity of Dinoroseobacter shibae for different membrane potential affecting agents.
Dang Nyguen (Research Project) 2015. Comparison of the membrane potential (Δψ)-indicating dyes JC-10 and DiOC2(3) by fluoresence microscopy
Conferences:
Kirchhoff C, Cypionka H; ISME 2016, Montreal. Membrane potential gives kick-off for quick ATP regeneration after short-term anoxia in Dinoroseobacter shibae
Kirchhoff C, Cypionka H; VAAM 2015, Marburg. Energetically depleted Dinoroseobacter shibae maintains strong membrane potential. poster
Kirchhoff C, Cypionka H; VAAM 2014, Dresden. Energetic state of Dinoroseobacter shibae during short-term anoxia. poster
Soora M, Cypionka H; VAAM 2013, Bremen. Light-enhanced survival of Dinoroseobacter shibae during long-term starvation. poster
Soora M, Cypionka H; VAAM 2011, Karlsruhe. Role of light in the survival of Dinoroseobacter shibae during starvation. poster
Ecological significance of secondary metabolite production by members of the Roseobacter clade
Supervisors: apl. Prof. Dr. Thorsten Brinkhoff and Prof. Dr. Meinhard Simon
Research associates: Dr. Marco Dogs, Dr. Martine Berger, Laura Wolter (PhD student), Sven Breider (PhD student), Sujatha Srinivas (master student), Agnes Picard (master student).
Former research associates (topics see below): Paul Beyersmann (dissertation finished 2016), Sebastian Thole (dissertation finished 2012), Daniela Kalhoefer (dissertation finished 2011), Sarah Hahnke (dissertation finished 2011), Regina Gohl (master thesis finished 2012), Susann Zilkenat (master thesis finished 2011), Sven Breider (master thesis finished 2011), Ines Preuth (diploma thesis finished 2010).
Aims
Bacteria of the Roseobacter clade appear worldwide in marine habitats, often in high abundances. Overall, these organisms show a high phylogenetic and metabolic diversity. The aim of this project is to identify and study members of the Roseobacter clade producing secondary metabolites and finally to elucidate the ecological significance of the compounds for these organisms. Besides the investigation of established model organisms, new strains are tested under various conditions to determine if and when secondary metabolites are produced. By screening a variety of isolates, clusters or groups with increased potential for secondary metabolite production will be identified. Genetic experiments with selected model organisms elucidate which genes and biochemical pathways are involved and how the production is controlled. Further experiments unravel interactions of roseobacters with other pro- and eukaryotic microorganisms.
Methods
To assess the diversity (mainly richness, but also abundance of the most relevant organisms) of the Roseobacter clade with respect to secondary metabolite producing species, we use culture-dependent and -independent approaches (DGGE based Roseobacter clade specific primers as well as 454 sequencing in collaboration with project A3). Isolates were obtained from various marine habitats, i.e. from surfaces, which provide environments ruled by strong competition (e.g. surfaces of macroalgae, see Figure 1), and for comparison also from pelagic systems (in collaboration with project A1). Identification of new strains is performed by analysis of their 16S rRNA genes. Subsequently, the strains are screened for production of secondary metabolites. Therefor, biological and chemical methods are applied, e.g. inhibtion tests against a broad range of microorganisms on agar plates, but also chemical methods in collaboration with colleagues from other projects of the TRR 51 (B3 and C2).
Fig. 1. Sampling site for various macroalgae at the coast of Galicia, Spain. Here we found a broad variety of different brown-, green- and red-algae, which were screened for the presence of Roseobacter clade bacteria. Sampling was done in collaboration with Prof. Juan Barja, University of Santiago de Compostela.
For deeper knowledge the genomes of some model organisms were sequenced and analysed (i.e. Phaeobacter and Roseobacter spp.). They provide now an excellent basis for genetic experiments, to elucidate which genes and biochemical pathways are involved in the production of the secondary metabolites and how the production is controlled. The latter is also studied by microarray-experiments in collaboration with project B4. These experiments are currently focussed on organisms of the genus Phaeobacter, for which production of various secondary metabolites has been demonstrated.
Further experiments unravel interactions of roseobacters with other pro- and eukaryotic microorganisms. Here we perform colonization experiments of green fluorescent protein (gfp)-labeled Phaeobacter gallaeciensis DSM 17395 cells, which showed settlement of the Phaeobacter cells on various organisms and surfaces (see Figure 2).
Fig. 2. Fluorescence microscopic images of gfp-labeled P. gallaeciensis cells proliferating on different surfaces. (a) Tissue sample of the macro alga Fucus spp., (b) aggregated cells of the dinoflagellate Alexandrium carterea, (c) culture of the diatom Thalassiosira rotula, (d) slice of crab tissue. Magnification 1000 fold. From Thole et al., 2012.
For Phaeobacter gallaeciensis DSM 17395 we established several genetic methods. Presumably most genes involved in the production of the antibiotic tropodithietic acid and several regulatory parameters were determined (see publications of project B2). It is planned to deepen the studies on this organism, but also to investigate other secondary metabolite producing roseobacters, recently isolated from macroalgae. One promising example is a strain obtained from Fucus spp., showing inhibiting properties only when Fucus material is present in the growth medium. Another secondary metabolite producing bacterium, isolated from the marine alga Ulva australis, was recently characterized and described as a new species of a new genus, Epibacterium ulvae (in collaboration with colleagues from the University of New South Wales, Sydney, Australia). The secondary metabolite production of this organism and the interaction with its host will also be further studied.
Publications
List of Publications (Project B2)
2017
Breider S, Freese HM, Spröer C, Simon M, Overmann J, Brinkhoff T (2017) Phaeobacter porticola sp. nov., an antibiotic producing bacterium isolated from a harbor in the southern North Sea. Int J Syst Evol Microbiol. In press.
Dogs M, Wemheuer B, Wolter L, Bergen N, Daniel R, Simon M, Brinkhoff T (2017) Rhodobacteraceae on the marine brown alga Fucus spiralis are predominant and show physiological adaptation to an epiphytic lifestyle. Syst Appl Microbiol, in press.
Beyersmann PG, Tomasch J, Son K, Stocker R, Göker M, Wagner-Döbler I, Simon M, Brinkhoff T (2017) Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci Rep 7: 730. 10.1038/s41598-017-00784-7 [doi];10.1038/s41598-017-00784-7 [pii].
Celik E, Maczka M, Bergen N, Brinkhoff T, Schulz S, Dickschat JS (2017) Metabolism of 2,3-dihydroxypropane-1-sulfonate by marine bacteria. Org Biomol Chem 15: 2919-2922.
Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, Klenk HP, Schomburg D, Petersen J, Göker M. (2017) Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME 11: 1483-1499.
2016
Giebel, H.-A., F. Klotz, S. Voget, A. Poehlein, K. Grosser, A. Teske, T. Brinkhoff. 2016. Draft genome sequence of the marine Rhodobacteraceae strain O3.65, cultivated from oil-polluted seawater of the Deepwater Horizon oil spill. Stand. Genomic Sci. 11: DOI: 10.1186/s40793-016-0201-7.
Billerbeck, S., B. Wemheuer, S. Voget, A. Poehlein, H.-A. Giebel, T. Brinkhoff, L. Gram, W. H. Jeffrey, R. Daniel, M. Simon. 2016. Biogeography and environmental genomics of CHAB-I-5, a pelagic lineage of the marine Roseobacter clade. Nature Microbiol. 1: Article Number: 16063.
Wichmann, H., T. Brinkhoff, M. Simon, C. Richter-Landsberg. 2016. Dimethyl-sulfoniopropionate promotes process outgrowth in neural cells and exerts protective effects against tropodithietic acid. Marine Drugs. 14: Article Number: UNSP 89.
2015
Wichmann, H., F. Vocke, T. Brinkhoff, M. Simon, C. Richter-Landsberg. 2015. Cytotoxic effects of tropodithietic acid on mammalian clonal cell lines of neuronal and glial origin. Marine Drugs. 13: 7113–7123.
Ziesche, L., H. Bruns, M. Dogs, L. Wolter, F. Mann, I. Wagner-Döbler, T. Brinkhoff,. S. Schulz. 2015. Homoserine lactones, methyl oligohydroxybutyrates and other extracellular metabolites of macroalgae associated bacteria of the Roseobacter clade: Identification and function. ChemBioChem. 16: 2094-2107.
Gram, L., B. Barker Rasmussen, B. Wemheuer, N. Bernbom, Y. Yin Ng, C. H. Porsby, S. Breider, T. Brinkhoff. 2015. Phaeobacter inhibens from the Roseobacter-clade has an environmental niche as surface colonizer in harbours. Syst. Appl. Microbiol. 7: 483-493.
Billerbeck, S., J. Orchard, B.J. Tindall, H.-A. Giebel, T. Brinkhoff, M. Simon. 2015. Description of Octadecabacter temperatus sp. nov., isolated from the southern North Sea, emended description of the genus Octadecabacter and reclassification of Octadecabacter jejudonensis (Park & Yoon, 2014) as Pseudooctadecabacter jejudonensis gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 65: 1967-1974.
Klingner, A., A. Bartsch, M. Dogs, I. Wagner-Döbler, D. Jahn, M. Simon, T. Brinkhoff, J. Becker, C. Wittmann. 2015. Large-scale 13C-flux profiling reveals conservation of the Entner-Doudoroff pathway as glycolytic strategy among glucose-using marine bacteria. Appl. Environ. Microbiol. 81: 2408-2422.
Voget, S., B. Wemheuer, T. Brinkhoff, J. Vollmers, S. Dietrich, H.A. Giebel, C. Beardsley, C. Sardemann, I. Bakenhus, S. Billerbeck, R. Daniel, M. Simon. 2015. Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J. 9: 371–384.
2014
Breider, S., C. Scheuner, P. Schumann, A. Fiebig, J. Petersen, S. Pradella, M. Simon, H.-P. Klenk, T. Brinkhoff, M. Göker. 2014. Genome-scale data suggest reclassifications in the Leisingera-Phaeobacter cluster including proposals for Sedimentitalea gen. nov. and Pseudophaeobacter gen. nov. Front. Microbiol. doi: 10.3389/fmicb.2014.00416.
Breider, S., H. Teshima, J. Petersen, O. Chertkov, H. Dalingault, A. Chen, A. Pati, N. Ivanova, A. Lapidus, L.A. Goodwin, P. Chain, J.C. Detter, M. Rohde, B.J. Tindall, N.C. Kyrpides, T. Woyke, M. Simon, M. Göker, H.-P. Klenk, T. Brinkhoff. 2014. Genome sequence of Leisingera nanhaiensis strain DSM 24252T isolated from marine sediment. Stand. Genomic Sci. 9: 687-703.
2013
Beyersmann PG, Chertkov O, Petersen J, Fiebig A, 11 co-authors, Simon M, Göker M, Klenk HP, Brinkhoff T (2013) Genome sequence of Phaeobacter caeruleus type strain (DSM 24564T), a surface-associated member of the marine Roseobacter clade. Stand Genomic Sci 8: 403-419.
Breider S, Teshima H, Petersen J, Fiebig A, 12 co-authors, Simon M, Göker M, Klenk HP, Brinkhoff T (2013) Complete genome sequence of Leisingera nanhaiensis strain DSM 24252T isolated from marine sediment. Stand Genomic Sci, 9: 687-703.
Brock NL, Citron CA, Zell C, Berger M, Wagner-Döbler I, Petersen J, Brinkhoff T, Simon M, Dickschat JS (2013) Isotopically labeled sulfur compounds and synthetic selenium and tellurium analogs to study sulfur metabolism in marine bacteria. Beilstein J. Org. Chem. 9: 942-950.
Buddruhs N, O. Chertkov, J. Petersen, A. Fiebig, A. Chen, A. Pati, N. Ivanova, A. Lapidus, L. Goodwin, P. Chain, J. Detter, S. Gronow, N. Kyrpides, T. Woyke, M. Göker, T. Brinkhoff, H.P. Klenk. 2013. Complete genome sequence of the marine methyl-halide oxidizing Leisingera methylohalidivorans type strain (DSM 14336T), a member of the Roseobacter clade. Stand. Genomic Sci. 9: 128-141 (doi: 10.4056/sigs.4297965).
Buddruhs N, Pradella S, Göker M, Päuker O, Michael V, Pukall R, Spröer C, Schumann P, Petersen J, Brinkhoff T (2013) Molecular and phenotypic analyses reveal the non-identity of the Phaeobacter gallaeciensis type strain deposits CIP 105210T and DSM 17395. Int. J. Syst. Evol. Microbiol. 63: 4340–4349.
Dogs M, Voget S, Teshima H, Petersen J, Fiebig A, 12 co-authors, Simon M, Klenk HP, Göker M, Brinkhoff T (2013) Genome sequence of Phaeobacter inhibens type strain (T5T), a secondary-metabolite producing member of the marine Roseobacter clade, and emendation of the species Phaeobacter inhibens. Stand Genomic Sci, 9: 334-350 DOI:10.4056/sigs.4448212).
Dogs M, Teshima H, Petersen J, Fiebig A, 13 co-authors, Simon M, Klenk HP, Göker M, Brinkhoff T (2013) Genome sequence of Phaeobacter daeponensis type strain (DSM 23529T), a facultatively anaerobic bacterium isolated from marine sediment, and emendation of Phaeobacter daeponensis. Stand Genomic Sci 9: 142-159.
Freese H, Dalingault H, Petersen J, Pradella S, Fiebig A, 12 co-authors, Brinkhoff T, Göker M, Overmann J, Klenk HP (2013) Genome sequence of the phage-gene rich marine Phaeobacter arcticus type strain DSM 23566T. Stand Genomic Sci 8(3): 450–464.
Giebel, H.-A., D. Kalhoefer, R. Gahl-Janssen, Y.-J. Choo, K. Lee, J.-C. Cho, B.J. Tindall, E. Rhiel, C. Beardsley, Ö.O. Aydogmus, S. Voget, R. Daniel, M. Simon, T. Brinkhoff. 2013. Planktomarina temperata gen. nov., sp. nov., belonging to the globally distributed RCA cluster of the marine Roseobacter clade, isolated from the German Wadden Sea. Int. J. Syst. Evol. Microbiol. 63: 4207–4217.
Hahnke S, Brock NL, Zell C, Simon M, Dickschat JS, Brinkhoff T (2013) Physiological diversity of Roseobacter clade bacteria co-occurring during a phytoplankton bloom in the North Sea. Syst Appl Microbiol 36: 39– 48.
Hahnke, S., M. Sperling, T. Langer, A. Wichels, G. Gerdts, C. Beardsley, T. Brinkhoff, M. Simon. 2013. Distinct seasonal growth patterns of the bacterium Planktotalea frisia in the North Sea and specific interaction with phytoplankton algae. FEMS Microbiol. Ecol. 86: 185-199.
Kalhoefer D, Thole S, Voget S, Lehmann R, Liesegang H, Wollher A, Daniel R, Simon M, Brinkhoff T (2011) Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis. BMC Genomics. DOI: 10.1186/1471-2164-12-324.
Penesyan A, Breider S, Schumann P, Tindall BJ, Egan S, Brinkhoff T (2013) Epibacterium ulvae gen. nov., sp. nov., epibiotic bacteria isolated from the surface of a marine alga. Int J Syst Evol Microbiol 63: 1589 - 1596.
Riedel, T., H. Teshima, J. Petersen, A. Fiebig, K. Davenport, H. Daligault, T. Erkkila, W. Gu, C. Munk, Y. Xu, A. Chen, A. Pati, N. Ivanova, L.A. Goodwin, P. Chain, J.C. Detter, M. Rohde, S. Gronow, N.C. Kyrpides, T. Woyke, M. Göker, T. Brinkhoff, H.-P. Klenk. 2013. Genome sequence of the Leisingera aquimarina type strain (DSM 24565T), a member of the marine Roseobacter clade rich in extrachromosomal elements. Stand. Genomic Sci. 8: 389-402.
Thole S, Kalhoefer D, Voget S, Berger M, Engelhardt T, Liesegang H, Wollher A, Kjelleberg S, Daniel R, Simon M, Thomas T, Brinkhoff T (2012) Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life. ISME J 6: 2229–2244.
Vollmers, J., S. Voget, S. Dietrich, K. Gollnow, M. Smits, K. Meyer, T. Brinkhoff, M. Simon, R. Daniel. 2013. Poles apart: Arctic and Antarctic Octadecabacter strains share high genome plasticity and a new type of xanthorhodopsin. PloS one. 8: e63422.
2012
Berger M, Brock NL, Liesegang H, Dogs M, Preuth I, Simon M, Dickschat JS, Brinkhoff T (2012) Genetic analysis of the upper phenylacetate catabolic pathway in the production of tropodithietic acid by Phaeobacter gallaeciensis. Appl Environ Microbiol 78: 3539-3551.
Thole, S, Kalhoefer D, Voget S, Berger M, Engelhardt T, Liesegang H, Wollherr A, Kjelleberg S, Daniel R, Simon M et al.. 2012. Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life.. The ISME journal. 6(12):2229-44.
Penesyan, A, Breider S, Schumann P, Tindall BJ, Egan S, Brinkhoff T. 2012. Epibacterium ulvae gen. nov., sp. nov., epibiotic bacteria isolated from the surface of a marine alga.. International journal of systematic and evolutionary microbiology.
2011
Berger M, Neumann A, Schulz S, Simon M, Brinkhoff T (2011) Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by n-acyl homoserine lactone-mediated quorum sensing. J Bacteriol 193: 6576–6585.
Kalhoefer, D, Thole S, Voget S, Lehmann R, Liesegang H, Wollher A, Daniel R, Simon M, Brinkhoff T. 2011. Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis.. BMC genomics. 12:324.
List of Publications (Further publications concerning the Roseobacter clade)
2013
Hahnke, S, Tindall BJ, Schumann P, Simon M, Brinkhoff T. 2013. Pelagimonas varians gen. nov., sp. nov., isolated from the southern North Sea.. International journal of systematic and evolutionary microbiology. 63(Pt 3):835-43.
2012
Hahnke, S, Tindall BJ, Schumann P, Sperling M, Brinkhoff T, Simon M. 2012. Planktotalea frisia gen. nov., sp. nov., isolated from the southern North Sea.. International journal of systematic and evolutionary microbiology. 62(Pt 7):1619-24.
Lenk, S, Moraru C, Hahnke S, Arnds J, Richter M, Kube M, Reinhardt R, Brinkhoff T, Harder J, Amann R et al.. 2012. Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes.. The ISME journal. 6(12):2178-87.
2011
Petersen, J, Brinkmann H, Berger M, Brinkhoff T, Päuker O, Pradella S. 2011. Origin and evolution of a novel DnaA-like plasmid replication type in Rhodobacterales.. Molecular biology and evolution. 28(3):1229-40.
Giebel, H-A, Kalhoefer D, Lemke A, Thole S, Gahl-Janssen R, Simon M, Brinkhoff T. 2011. Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate.. The ISME journal. 5(1):8-19.
2010
Zhao, C, Burchardt M, Brinkhoff T, Beardsley C, Simon M, Wittstock G. 2010. Microfabrication of patterns of adherent marine bacterium Phaeobacter inhibens using soft lithography and scanning probe lithography.. Langmuir : the ACS journal of surfaces and colloids. 26(11):8641-7.
Thiel, V, Brinkhoff T, Dickschat JS, Wickel S, Grunenberg J, Wagner-Döbler I, Simon M, Schulz S. 2010. Identification and biosynthesis of tropone derivatives and sulfur volatiles produced by bacteria of the marine Roseobacter clade.. Organic & biomolecular chemistry. 8(1):234-46.
Wagner-Döbler, I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G et al.. 2010. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea.. The ISME journal. 4(1):61-77.
2009
Zech, H, Thole S, Schreiber K, Kalhöfer D, Voget S, Brinkhoff T, Simon M, Schomburg D, Rabus R. 2009. Growth phase-dependent global protein and metabolite profiles of Phaeobacter gallaeciensis strain DSM 17395, a member of the marine Roseobacter-clade.. Proteomics. 9(14):3677-97.
Giebel, H-A, Brinkhoff T, Zwisler W, Selje N, Simon M. 2009. Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean.. Environmental microbiology. 11(8):2164-78.
2008
Brinkhoff, T, Giebel H-A, Simon M. 2008. Diversity, ecology, and genomics of the Roseobacter clade: a short overview.. Archives of microbiology. 189(6):531-9.
2007
Martens, T, Gram L, Grossart H-P, Kessler D, Müller R, Simon M, Wenzel SC, Brinkhoff T. 2007. Bacteria of the Roseobacter clade show potential for secondary metabolite production.. Microbial ecology. 54(1):31-42.
2006
Martens, T, Heidorn T, Pukall R, Simon M, Tindall BJ, Brinkhoff T. 2006. Reclassification of Roseobacter gallaeciensis Ruiz-Ponte et al. 1998 as Phaeobacter gallaeciensis gen. nov., comb. nov., description of Phaeobacter inhibens sp. nov., reclassification of Ruegeria algicola (Lafay et al. 1995) .... International journal of systematic and evolutionary microbiology. 56(Pt 6):1293-304.
2004
Selje, N, Simon M, Brinkhoff T. 2004. A newly discovered Roseobacter cluster in temperate and polar oceans.. Nature. 427(6973):445-8.
Brinkhoff, T, Bach G, Heidorn T, Liang L, Schlingloff A, Simon M. 2004. Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates.. Applied and environmental microbiology. 70(4):2560-5.
Completed Master- and PhD-thesis within project B2
Martine Berger (PhD thesis). 2012. Genome-based investigations of the secondary metabolism of representatives of the Roseobacter clade and genetic analyses of the biosynthesis and regulation of tropodithietic acid production.
Sebastian Thole (PhD thesis). 2012. Comparative and functional genome analysis of two closely related Phaeobacter gallaeciensis strains and other host-associated Roseobacter clade members.
Daniela Kalhoefer (PhD thesis). 2011. Genome analysis and comparative genomics of host-associated bacteria of the marine Roseobacter clade.
Sarah Hahnke (PhD thesis). 2011. Physiological characterization and molecular ecological investigation of diverse organisms of the Roseobacter clade isolated from the North Sea.
Regina Gohl (Master thesis). 2012. Analysis of the diversity of algae associated organisms of the Roseobacter clade.
Susann Zilkenat (Master thesis). 2011. Characterization of the putative siderophore synthesis genes RRGA03155 and RRGA03157 of Phaeobacter gallaeciensis DSM 17395.
Sven Breider (Master thesis). 2011. Characterization of two epibiotic bacterial strains of the new genus Epibacterium isolated from the marine seaweed Ulva australis.
Ines Preuth (Diploma). 2010. Regulation der Tropodithietsäure-Produktion bei Phaeobacter gallaeciensis DSM 17395 in Abhängigkeit vom Substrat.
Contributions to conferences
Beyersmann, P., M. Berger, J. Tomasch, I. Wagner-Döbler, M. Simon, T. Brinkhoff. 2013. The antibiotic tropodithietic acid can replace acylated homoserine lactone as global gene regulator in Phaeobacter sp. DSM 17395. VAAM, Bremen, Germany. Oral presentation.
Wolter, L.A., R. Gohl, M. Dogs, M. Simon, T. Brinkhoff. 2013. Specific epibacterial communities on marine macroalgae: distribution patterns of the Roseobacter clade. VAAM, Bremen, Germany. Poster presentation.
Dogs, M., P. Beyersmann , T. Brinkhoff. 2012. Progress Report and Future Perspectives. 7th Status Seminar of the Transregio 51, Hanse Wissenschaftskolleg, Delmenhorst, Germany. Oral presentation.
Beyersmann, P., M. Simon, T. Brinkhoff. 2012. Investigation of biosynthesis and regulation of secondary metabolite production in Phaeobacter gallaeciensis (DSM 17395). 7th Status Seminar of the Transregio 51, Hanse Wissenschaftskolleg, Delmenhorst, Germany. Oral presentation.
Dogs, M., V. Lünsmann, R. Gohl, B. Wemheuer, S. Voget, R. Daniel, M. Simon, T. Brinkhoff. 2012. Specific epibacterial community on marine macroalgae: distribution pattern of the Roseobacter clade. ASM, San Francisco, USA. Poster presentation.
Beyersmann, P., M. Berger, J. Tomasch, I. Wagner-Döbler, M. Simon, T. Brinkhoff. 2012. AHL mediated quorum sensing in Phaeobacter gallaeciensis. ASM, San Francisco, USA. Poster presentation.
Dogs, M., V. Lünsmann, R. Gohl, B. Wemheuer, S. Voget, R. Daniel, M. Simon, T. Brinkhoff. 2012. Specific epibacterial community on marine macroalgae: secondary metabolite production of the Roseobacter clade. VAAM International Workshop, Braunschweig, Germany. Oral presentation.
Beyersmann, P., M. Berger, J. Tomasch, I. Wagner-Döbler, M. Simon, T. Brinkhoff. 2012. Microarray analysis: quorum sensing regulates expression of a large part of the Phaeobacter gallaeciensis genome. VAAM International Workshop, Braunschweig, Germany. Oral presentation.
Dogs, M., T. Brinkhoff. 2012. Specific epibacterial communities of the Roseobacter clade on marine macroalgae. 6th Status Seminar of the Transregio 51, HZI Braunschweig, Germany. Oral presentation.
Beyersmann, P., M. Simon, T. Brinkhoff. 2012. Investigation of biosynthesis and regulation of secondary metabolite production in Phaeobacter gallaeciensis (DSM 17395). 6th Status Seminar of the Transregio 51, HZI Braunschweig, Germany. Oral presentation.
Dogs, M., T. Brinkhoff. 2011. Ecological significance of secondary metabolite production by members of the Roseobacter clade. 5th Status Seminar of the Transregio 51, Oldenburg, Germany. Oral presentation.
Beyersmann, P., M. Simon, T. Brinkhoff. 2011. Investigation of biosynthesis and regulation of secondary metabolite production in Phaeobacter gallaeciensis (DSM 17395). 5th Status Seminar of the Transregio 51, Oldenburg, Germany. Oral presentation.
Dogs, M., M. Simon, T. Brinkhoff. 2011. Detection of specific epibacterial communities affiliated to the marine Roseobacter group reflects adaptation to various macroalgae. VAAM, Karlsruhe, Germany. Poster presentation.
Beyersmann, P., M. Berger, S. Thole, M. Simon, T. Brinkhoff. 2011. Investigation of biosynthesis, function and significance of siderophores in Phaeobacter gallaeciensis. VAAM, Karlsruhe, Germany. Poster presentation.
Berger, M., A. Neumann, M. Dogs1, I. Preuth, S. Schulz, M. Simon, T. Brinkhoff. 2011. Quorum‐sensing control of tropodithietic acid biosynthesis in Phaeobacter gallaeciensis. VAAM, Karlsruhe, Germany. Poster presentation.
Simon, M., S. Hahnke, H.-A. Giebel, H. Osterholz, H. Simon, M. Sperling, T. Brinkhoff. 2011. Physiology and interactions of phytoplankton-associated roseobacters. SAME; Rostock/Warnemünde, Germany. Oral presentation.
Berger, M., H. Liesegang, M. Simon, T. Brinkhoff. 2010. Enzyme with homology to archaeal indolepyruvate oxidoreductase (IOR) is involved in tropodithietic acid (TDA) production and phenylalanine metabolism of Phaeobacter gallaeciensis. Kick Off Symposium of the Transregional Collaborative Research Center (TRR 51). Hansewissenschaftskolleg, Delmenhorst, Germany. Oral presentation.
Hahnke, S., H.-A. Giebel, M.Sperling, M. Simon, T. Brinkhoff. 2010. Physiology and biogeography of phytoplankton-associated roseobacters. Kick-off Symposium of the Transregional Collaborative Research Center; Delmenhorst, Germany. Oral presentation.
Simon, M., S. Hahnke, H.-A. Giebel, H. Osterholz, M. Sperling, T. Brinkhoff. 2010. Physiology and biogeography of phytoplankton-associated roseobacters. Workshop: The microbial view of marine biogeochemical cycles; Banyuls, France. Oral presentation.
Biosynthetic pathways to secondary metabolites of the Roseobacter clade
this project has been transferred to B7
Supervisor: J. S. Dickschat, University Bonn (https://www.chemie.uni-bonn.de/oc/forschung/arbeitsgruppen/ak_dickschat/prof.-dr.-jeroen-s.-dickschat)
Scientists: N. L. Brock, P. Rabe, R. Riclea
Objectives
Bacteria of the Roseobacter clade constitute one of the most important groups of marine bacteria. Genetic information reveals the importance of two pathways, i.e. sulfur metabolism—especially the degradation of dimethylsulfoniopropionate (DMSP) —and phenylacetate degradation. Both will be investigated in the two model organisms using a gene knockout approach in combination with feeding experiments. Both pathways cumulate in the biosynthesis of the antibiotic tropodithietic acid (TDA) that will be investigated in detail, flanked by studies towards the total synthesis of TDA and biosynthetic intermediates. Genetic information suggest that further secondary metabolites are produced, that will be identified.
Methods
The closed-loop stripping apparatus (CLSA) is a powerful tool for the investigation of volatiles from microorganisms. Bacterial cultures can be embedded in a glass vessel together with a charcoal filter. A continuous airstream is circulated through the apparatus. Volatiles that are emitted by the bacteria are trapped and enriched on the charcoal filter over 24 hours and can subsequently be eluted with an organic solvent. Analysis of these headspace extracts via GC-MS gives access to easy and high throughput compound identification by comparison of mass spectra to data bases. For unknown constituents of the headspace extract, structural proposals can be deduced from these mass spectra that need to be verified by total synthesis of a reference compound. Furthermore, isotopically labeled metabolites can be chemically synthesized and used in feeding experiments with the bacteria. Incorporation of label into volatile secondary metabolites can be monitored by the CLSA/GC-MS method as isotopic shifts will be observed in the mass-spectra. This allows in many cases for valuable conclusions about the underlying biosynthetic machinery. Moreover, gene knockouts of genes from a cluster that is crucial for the production of a certain metabolite can result in the accumulation of pathway intermediates which will allow for the reconstruction of the pathway and the identification of all its intermediates.
Publications
2017
Burkhardt I, Lauterbach L, Brock NL, Dickschat JS (2017) Chemical Differentiation of Three DMSP Lyases from the Marine Roseobacter group. Org Biomol Chem (published online, doi: 10.1039/C7OB00913E).
Celik E, Maczka M, Bergen N, Brinkhoff T, Schulz S, Dickschat JS (2017) Metabolism of 2,3-dihydroxypropane-1-sulfonate by marine bacteria. Org Biomol Chem 15: 2919-2922.
2016
Widderich N, Czech L, Elling FJ, Könneke M, Stöveken N, Pittelkow M, Riclea R, Dickschat JS, Heider J, Bremer E (2016a) Strangers in the archaeal world: Osmostress-responsive biosynthesis of ectoine and hydroxyectoine by the marine thaumarchaeon Nitrosopumilus maritimus. Environ Microbiol 18:1227-1248.
Widderich N, Kobus S, Höppner A, Riclea R, Seubert A, Dickschat JS, Heider J, Smits SHJ, Bremer E (2016b) Biochemistry and Crystal Structure of Ectoin Synthase: a Metal-Containing Member of the Cupin Superfamily. PLoS ONE 11:e0151285.
2015
Broy S, Chen C, Hoffmann T, Brock NL, Nau-Wagner G, Jebbar M, Smits SHJ, Dickschat JS, Bremer E (2015) Abiotic Stress Protection by Ecologically Abundant DMSP and its Natural and Synthetic Derivatives: Insights from Bacillus subtilis. Environ Microbiol 17:2362-2378.
Dickschat JS, Rabe P, Citron C (2015) The chemical biology of dimethylsulfoniopropionate. Org Biomol Chem 13:1954-1968.
2014
Brock NL, Nikolay A, Dickschat JS (2014) Biosynthesis of the Antibiotic Tropodithietic Acid by the Marine Bacterium Phaeobacter inhibens. ChemComm 50:5487-5489.
Rabe P, Klapschinski TA, Brock NL, Citron CA, D'Alvise P, Gram L, Dickschat JS (2014) Synthesis and Bioactivity of Analogs of the Marine Antibiotic Tropodithietic Acid. Beilstein J Org Chem 10: 1796-1801.
2013
Berger M, Brock NL, Liesegang H, Dogs M, Simon M, Dickschat JS, Brinkhoff T (2012) Genetic Analysis of the Upper Phenylacetate Catabolic Pathway in the Production of Tropodithietic Acid by Phaeobacter gallaeciensis. Appl Environ Microbiol 78:3539-3551.
Brock NL, Citron CA, Zell C, Berger M, Wagner-Döbler I, Petersen J, Brinkhoff T, Simon M, Dickschat JS (2013) Isotopically Labeled Sulfur Compounds and Synthetic Selenium and Tellurium Analogs to Study Sulfur Metabolism in Marine Bacteria. Beilstein J Org Chem 9:942-950.
Hahnke S, Brock NL, Zell C, Simon M, Dickschat JS, Brinkhoff T (2013) Physiological diversity of Roseobacter clade bacteria co-occurring during a phytoplankton bloom in the North Sea. Syst Appl Microbiol 36:39-48.
Kielkowsky P, Brock NL, Dickschat JS, Hocek M (2013) Nucleobase Protection Strategy for Gene Cloning and Expression. ChemBioChem, 14:801-804.
Riclea R, Gleitzmann J, Bruns H, Junker C, Schulz B, Dickschat JS (2012) Algicidal Lactones from the Marine Roseobacter Clade Bacterium Ruegeria pomeroyi. Beilstein J Org Chem 8:941-950.
2012
Berger, M, Brock NL, Liesegang H, Dogs M, Preuth I, Simon M, Dickschat JS, Brinkhoff T. 2012. Genetic analysis of the upper phenylacetate catabolic pathway in the production of tropodithietic acid by Phaeobacter gallaeciensis.. Applied and environmental microbiology. 78(10):3539-51.
Riclea, R, Gleitzmann J, Bruns H, Junker C, Schulz B, Dickschat JS. 2012. Algicidal lactones from the marine Roseobacter clade bacterium Ruegeria pomeroyi.. Beilstein journal of organic chemistry. 8:941-50.
2010
Thiel, V, Brinkhoff T, Dickschat JS, Wickel S, Grunenberg J, Wagner-Döbler I, Simon M, Schulz S. 2010. Identification and biosynthesis of tropone derivatives and sulfur volatiles produced by bacteria of the marine Roseobacter clade.. Organic & biomolecular chemistry. 8(1):234-46.
Dickschat, JS, Zell C, Brock NL. 2010. Pathways and substrate specificity of DMSP catabolism in marine bacteria of the Roseobacter clade.. Chembiochem : a European journal of chemical biology. 11(3):417-25.
Schulz, S, Dickschat JS, Kunze B, Wagner-Dobler I, Diestel R, Sasse F. 2010. Biological activity of volatiles from marine and terrestrial bacteria.. Marine drugs. 8(12):2976-87.
2005
Dickschat, JS, Wagner-Döbler I, Schulz S. 2005. The chafer pheromone buibuilactone and ant pyrazines are also produced by marine bacteria.. Journal of chemical ecology. 31(4):925-47.
Cell-cell communication of bacteria from the Roseobacter group with other bacteria and algae
Supervisor: Prof. Dr. Wagner-Döbler
Scientists and students: Mathias Milici (PhD); Diana Patzelt (PhD); Hui Wang (PhD); Ina Buchholz (PhD); Dr. Jürgen Tomasch (Postdoc)
Aim
Cell-cell communication transforms clonal populations of bacteria into highly complex, well adapted communities. Here we unravel the quorum sensing (QS) regulon of the model organism Dinoroseobacter shibae and study interactions between Roseobacter bacteria and their eukaryotic host organisms.
Fig. 1. D. shibae populations show different mechanisms of cell division: Some cells divide by budding, other show symmetrical binary fission. The picture shows the wild-type. If the quorum sensing system is silenced, this morphological heterogeneity is lost. (Time lapse microscopy; Patzelt et al., submitted).
Fig.2. D. shibae and the algae Isochrysis galbana in co-culture. The bacteria carry a reporterplasmid for signalling molecules (acylated homoserine lactones, AHLs). Green fluorescence indicates synthesis of AHLs by the bacteria. Only a fraction of the population produces AHLs (Buchholz, unpublished).
Methods
D. shibae has a complex QS regulon comprised of three LuxI-type synthases and 5 LuxR-type transcriptional regulators. We are constructing knock-out mutants for these key genes and study their phenotype (growth, cell division, morphology, flagellae) and gene expression (microarrays and RNAseq). Population heterogeneity is analysed using time-lapse microscopy of strains that have been tagged with gfp or mcherry proteins for the promoter of interest, as well as FACS (fluorescence activated cell sorting). Using chemically synthesized autoinducers, we study the response of D. shibae to self-produced signals and to signals produced by other bacteria.
The interactions between algae and bacteria are studied in cultures of the dinoflagellate Prorocentrum minimum which is free of bacteria (axenic). This culture is inoculated with D. shibae and grows in a defined mineral medium (L1) without carbon source and without vitamin B12. Thus, algae and bacteria are critically dependent on each other: The heterotrophic bacteria require the products of algal photosynthesis, and the algae need the essential vitamin B12 which is synthesized by the bacteria.
Sampling with FS Polarstern in the Southern Ocean
Hui Wang and Irene Wagner-Döbler participated in cruise ANT28 into the Southern ocean as part of the Roseobacter group, joining cruise leg ANT28-4 (13th March – 9th April 2012, Punta Arenas – Punta Arenas) and cruise leg ANT28-5 (11th April – 16th May 2012, Punta Arenas – Bremerhaven). Water samples were obtained along a geographical gradient from defined depths. The water was filtered through membrane filters of 8 µm, 3 µm and 0,22 µm pore width. The filters were stored at -80°C. About 900 filters have been obtained. It is planned to investigate the microbiome and metatranscriptome with a focus on the interactions between algae and bacteria.
Fig. 3. The CTD (conductivity-temperature-depth instrument) is back on board. Water samples are filled into bottles. Polarstern, april 2012.
Publications
2017
Beyersmann PG, Tomasch J, Son K, Stocker R, Göker M, Wagner-Döbler I, Simon M, Brinkhoff T (2017) Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci Rep 7: 730. 10.1038/s41598-017-00784-7 [doi];10.1038/s41598-017-00784-7 [pii].
Petersen J, Wagner-Döbler I (2017) Plasmid transfer in the ocean - a case study from the Roseobacter group. Front Microbiol, accepted.
Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, Klenk HP, Schomburg D, Petersen J, Göker M. (2017) Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME 11: 1483-1499.
2016
Patzelt D, Michael V, Päuker O, Ebert M, Tielen P, Jahn D, Tomasch J, Petersen J, Wagner-Döbler I (2016) Gene flow across genus barriers - Conjugation of Dinoroseobacter shibae’s 191-kb killer plasmid into Phaeobacter inhibens and AHL-mediated expression of type IV secretion systems. Front Microbiol 7: 742.
Wagner-Döbler I (2016) Biofilm transplantation in the deep sea. Mol Ecol 25: 1905-1907. 10.1111/ mec.13612 [doi].
2015
Klingner A, Bartsch A, Dogs M, Wagner-Döbler I, Jahn D, Simon M, Brinkhoff T, Becker J, Wittmann C (2015) Large-scale 13C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose. Appl Environ Microbiol 81/7: 2408-2422.
Soora, M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, Wagner-Döbler I, Cypionka H (2015) Oxidative stress and starvation in Dinoroseobacter shibae: the role of extrachromosomal elements. Frontiers in microbiology. 6:233.
Voget S, Bruns H, Wagner-Döbler I, Schulz S, Daniel R (2015) Draft Genome Sequence of Roseovarius tolerans EL-164, a Producer of N-Acylated Alanine Methyl Esters and N-Acylhomoserine Lactones. Genome Announcement 3(5):15.
Wang H, Tomasch J, Michael V, Bhuju S, Jarek M, Petersen J, Wagner-Döbler I (2015) Identification of genetic modules mediating the Jekyll and Hyde interaction of Dinoroseobacter shibae with the dinoflagellate Prorocentrum minimum. Front Microbiol 6: 1262.
Ziesche L, Bruns H, Dogs M, Wolter L, Mann F, Wagner-Döbler I, Brinkhoff T, Schulz S (2015) Homoserine lactones, methyl oligohydroxybutyrates and other extracellular metabolites of macroalgae associated bacteria of the Roseobacter clade: Identification and function. ChemBioChem. 16: 2094-2107.
2014
Wang H, Tomasch J, Jarek M, Wagner-Döbler I (2014) A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates. Front Microbiol 5: 311. 10.3389/ fmicb.2014.00311 [doi].
Wang H, Ziesche L, Frank O, Michael V, Martin M, Petersen J, Schulz S, Wagner-Döbler I, Tomasch J (2014) The CtrA phosphorelay integrates differentiation and communication in the marine alphaproteobacterium Dinoroseobacter shibae. BMC Genomics 15: 130.
2013
Brock NL, Citron, CA, Zell, C, Berger, M, Wagner-Döbler, I, Petersen, J et al. (2013) Isotopically Labeled Sulfur Compounds and Synthetic Selenium and Tellurium Analogs to Study Sulfur Metabolism in Marine Bacteria. Beilstein J Org Chem 9:942-950.
Bruns, H, Thiel V, Voget S, Patzelt D, Daniel R, Wagner-Döbler I, Schulz S (2013) N-acylated alanine methyl esters (NAMEs) from Roseovarius tolerans, structural analogs of quorum-sensing autoinducers, N-acylhomoserine lactones. Chemistry & biodiversity. 10(9):1559-73.
Fiebig, A, Pradella S, Petersen J, Michael V, Päuker O, Rohde M, Göker M, Klenk H-P, Wagner-Döbler I (2013) Genome of the marine alphaproteobacterium Hoeflea phototrophica type strain (DFL-43(T)). Standards in genomic sciences. 7(3):440-8.
Fiebig, A, Pradella S, Petersen J, Päuker O, Michael V, Lünsdorf H, Göker M, Klenk H-P, Wagner-Döbler I (2013) Genome of the R-body producing marine alphaproteobacterium Labrenzia alexandrii type strain (DFL-11(T)). Standards in genomic sciences. 7(3):413-26.
Neumann, A, Patzelt D, Wagner-Döbler I, Schulz S (2013) Identification of new N-acylhomoserine lactone signalling compounds of Dinoroseobacter shibae DFL-12(T) by overexpression of luxI genes. Chembiochem 14/17: 2355-2361.
Patzelt, D, Wang H, Buchholz I, Rohde M, Gröbe L, Pradella S, Neumann A, Schulz S, Heyber S, Münch K et al. (2013) You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae. The ISME journal. 7(12):2274-86.
Pradella S, Petersen, J, Päuker, O, Michael, V, Lünsdorf, H, Göker, M et al. and Wagner-Döbler I (2013) Genome of the R-Body Producing Marine Alphaproteobacterium Labrenzia Alexandrii Type Strain (DFL-11T). Standards in Genomic Sciences 7(3).
Riedel, T, Rohlfs M, Buchholz I, Wagner-Döbler I, Reck M (2013) Complete sequence of the suicide vector pJP5603. Plasmid. 69(1):104-7.
Riedel, T, Gómez-Consarnau L, Tomasch J, Martin M, Jarek M, González JM, Spring S, Rohlfs M, Brinkhoff T, Cypionka H et al. (2013) Genomics and physiology of a marine flavobacterium encoding a proteorhodopsin and a xanthorhodopsin-like protein. PloS one. 8(3):e57487.
Riedel, T, Gómez-Consarnau L, Tomasch J, Martin M, Jarek M, González JM, Spring S, Rohlfs M, Brinkhoff T, Cypionka H et al. (2013) Genomics and physiology of a marine flavobacterium encoding a proteorhodopsin and a xanthorhodopsin-like protein. PloS one. 8(3):e57487.
Brock, NL, Citron CA, Zell C, Berger M, Wagner-Döbler I, Petersen J, Brinkhoff T, Simon M, Dickschat JS (2013) Isotopically labeled sulfur compounds and synthetic selenium and tellurium analogues to study sulfur metabolism in marine bacteria. Beilstein journal of organic chemistry. 9:942-50.
2012
Brinkhoff, T, Fischer D, Vollmers J, Voget S, Beardsley C, Thole S, Mussmann M, Kunze B, Wagner-Döbler I, Daniel R et al. (2012) Biogeography and phylogenetic diversity of a cluster of exclusively marine myxobacteria. The ISME journal. 6(6):1260-72.
2011
Jaramillo-Colorado B, Olivero-Verbel J, Stashenko EE, Wagner-Döbler I, Kunze B (2011) Anti-Quorum Sensing Activity of Essential Oils From Colombian Plants. Nat Prod Res 26(12):1075-86.
Lemme A, Gröbe L, Reck M, Tomasch J, Wagner-Döbler I (2011) Subpopulation-Specific Transcriptome Analysis of Competence-Stimulating-Peptide-Induced Streptococcus Mutans. J Bacteriol 193(8):1863-77.
Tomasch J, Gohl R, Bunk B, Diez M S, Wagner-Döbler I (2011) Transcriptional response of the photoheterotrophic marine bacterium Dinoroseobacter shibae to changing light regimes. The ISME journal. 5(12):1957-68.
2010
Riedel T, Tomasch J, Buchholz I, Jacobs J, Kollenberg M, Gerdts G, Wichels A, Brinkhoff T, Cypionka H, Wagner-Döbler I (2010) Constitutive expression of the proteorhodopsin gene by a flavobacterium strain representative of the proteorhodopsin-producing microbial community in the North Sea. Applied and environmental microbiology. 76(10):3187-97.
Riedel T, Tomasch J, Buchholz I, Jacobs J, Kollenberg M, Gerdts G, Wichels A, Brinkhoff T, Cypionka H, Wagner-Döbler I (2010) Constitutive expression of the proteorhodopsin gene by a flavobacterium strain representative of the proteorhodopsin-producing microbial community in the North Sea. Applied and environmental microbiology. 76(10):3187-97.
Thiel V, Brinkhoff T, Dickschat JS, Wickel S, Grunenberg J, Wagner-Döbler I, Simon M, Schulz S (2010) Identification and biosynthesis of tropone derivatives and sulfur volatiles produced by bacteria of the marine Roseobacter clade. Organic & biomolecular chemistry. 8(1):234-46.
Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G et al. (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. The ISME journal. 4(1):61-77.
2009
Thiel V, Kunze B, Verma P, Wagner-Döbler I, Schulz S (2009) New structural variants of homoserine lactones in bacteria.. Chembiochem : a European journal of chemical biology. 10(11):1861-8.
Thiel V, Vilchez R, Sztajer H, Wagner-Döbler I, Schulz S (2009) Identification, quantification, and determination of the absolute configuration of the bacterial quorum-sensing signal autoinducer-2 by gas chromatography-mass spectrometry.. Chembiochem : a European journal of chemical biology. 10(3):479-85.
Fürch T, Preusse M, Tomasch J, Zech H, Wagner-Döbler I, Rabus R, Wittmann C (2009) Metabolic fluxes in the central carbon metabolism of Dinoroseobacter shibae and Phaeobacter gallaeciensis, two members of the marine Roseobacter clade. BMC microbiology. 9:209.
2008
Bodor A, Elxnat B, Thiel V, Schulz S, Wagner-Döbler I (2008) Potential for luxS related signalling in marine bacteria and production of autoinducer-2 in the genus Shewanella. BMC microbiology. 8:13.
Pommerenke C, Gabriel I, Bunk B, Münch R, Haddad I, Tielen P, Wagner-Döbler I, Jahn D (2008) ROSY--a flexible and universal database and bioinformatics tool platform for Roseobacter related species. In silico biology. 8(2):177-86.
2007
Vilchez R, Lemme A, Thiel V, Schulz S, Sztajer H, Wagner-Döbler I (2007) Analysing traces of autoinducer-2 requires standardization of the Vibrio harveyi bioassay. Analytical and bioanalytical chemistry. 387(2):489-96.
2006
Wagner-Döbler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annual review of microbiology. 60:255-80.
2005
Biebl H, Allgaier M, Lünsdorf H, Pukall R, Tindall BJ, Wagner-Döbler I (2005) Roseovarius mucosus sp. nov., a member of the Roseobacter clade with trace amounts of bacteriochlorophyll a. International journal of systematic and evolutionary microbiology. 55(Pt 6):2377-83.
Biebl H, Allgaier M, Tindall BJ, Koblizek M, Lünsdorf H, Pukall R, Wagner-Döbler I (2005) Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. International journal of systematic and evolutionary microbiology. 55(Pt 3):1089-96.
PhD thesis
Ina Buchholz: Quorum Sensing in Dinoroseobacter shibae DFL-12T and its possible role in algae symbiosis. Dissertation TU Braunschweig, 19.09.2011
Contributions to conferences
Patzelt D, Wang H, Buchholz I, Rohde M, Gröbe L, Neumann A, Pradella S, Schulz S, Münch K, Jahn D, Wagner-Döbler I, and Tomasch J (2013) You are what you talk: Quorum sensing induces individualisation in the algal symbiont Dinoroseobacter shibae DFL-12. VAAM Bremen, 10.-13. March 2013 (Talk)
Beyersmann P, Berger M, Tomasch J, Wagner-Döbler I, Simon M, and Brinkhoff T (2013) The antibiotic tropodithietic acid can replace acylated homoserine lactone as global gene regulator in Phaeobacter sp. DSM 17395. VAAM Bremen, 10.-13. March 2013 (Talk)
Wang H, Tomasch J, Jarek M, and Wagner-Döbler I (2013) Understanding the relationship between Roseobacters and Dinoflagellates . VAAM Bremen, 10.-13. March 2013 (Poster)
Wagner-Döbler I (2012) B4: Progress report and future perspectives. 7th Status Seminar of the Transregio 51, 12-13. October 2012, Hanse Wissenschaftskolleg, Delmenhorst (Talk)
Tomasch J, Patzelt D, Wang H, Buchholz I, Gröbe L, Lünsdorf H, Wagner-Döbler I (2012) Quorum sensing controls population heterogeneity in the marine bacterium Dinoroseobacter shibae. ISME 14 19-24 August 2012, Copenhagen (Poster)
Patzelt D (2012) Quorum sensing controls virulence related traits and population heterogeneity in Dinoroseobacter shibae. 6th Status Seminar of the Transregio 51, 5th June 2012, HZI Braunschweig (Talk)
Tomasch J, Wang H, Buchholz I and Wagner-Döbler I (2011) Statistische Analyse der morphologischen Heterogenität bakterieller Kulturen. Biostats – Biologie und Statistik in der Praxis, 22-24. März 2011, Deutsche Sammlung für Mikroorganismen und Zellkulturen, Brauschweig (Poster)
Buchholz I, Gohl R and Wagner-Döbler I (2010) The production of autoinducer signals of D. shibae DFL-12T during cocultivation reveals the important role of quorum sensing in algae symbiosis. Kick-off Symposium of the Transregio 51, 13th -15th June 2010, Hanse Wissenschaftskolleg, Delmenhorst (Talk)
Buchholz I, Gohl R and Wagner-Döbler I (2010) The production of autoinducer signals of D. shibae DFL-12T during cocultivation reveals the important role of quorum sensing in algae symbiosis. VAAM Hannover, 28.-31 March 2010 (Poster)
Invited Talks
Wagner-Döbler I (2011) Symbiotic interactions: microbes in macrobes. Gordon Research Conference „Applied and Environmental Microbiology“, 10th – 15th July, 2011, Mount Holyoke College, MA, USA.
Wagner-Döbler I (2011) Global transcriptome analysis of the response to light and quorum sensing signals in a marine Roseobacter strain – sustainable use of energy on a global scale. Mikrobiologisches Kolloquium der Universität Jena, 13th April, 2011, Jena.
Wagner-Döbler I (2010) Global transcriptome analysis of the response to light and quorum sensing signals in a marine Roseobacter strain. Mikrobiologisches Kolloquium, Universität Mainz, 6th December 2010 (invitation by Prof. Dr. G. Unden).
Common regulatory networks for the adaptation to low iron and oxygen tension
Principal investigators: Prof. Dr. Dieter Jahn, Dr. Elisabeth Härtig
PhD student: Maren Behringer, Miriam Becker
Objective
Dinoroseobacter shibae belongs to the abundant and ecological important marine Roseobacter clade. The bacterium is able to generate energy by anaerobic respiration via denitrification. Moreover, it performs arginine and pyruvate fermentation to sustain anaerobic long-time survival. The adaptation to changing oxygen concentrations is controlled via a fine-tuned regulatory network involving the oxygen-sensing regulator Fnr and several Dnrs organized in regulatory cascades. The anaerobic regulation is closely connected to iron acquisition, though the anaerobic regulators depend on Fe-containing [FeS]-cluster or heme as cofactors. Three potential iron-dependent regulators were found in the D. shibae genome: Fur, Irr and RirA. Using genetic techniques and transcriptome analyses we aim to identify the stimuli of the involved regulators and target regulons and to understand the interplay with the networks for the response to oxygen depletion, nitrate, carbon sources and different stresses.
Projects
Regulation of respiratory pathways for the energy generation in Dinoroseobacter shibae
Objectives
We analyzed the role of the four regulators FnrL, DnrD, DnrF and DnrE of D. shibae in regulating genes encoding nitrate respiration and denitrification pathways. Moreover, we studied low oxygen tension and NO as signals for anaerobic gene expression.
Material & Methods
Knockout mutant strains for fnrL, dnrD, dnrF and dnrE of D. shibae were generated. We defined the regulons by comparing transcript levels of the regulatory mutant strains with the D. shibae wild type strain after shift from aerobic to anaerobic growth conditions. After regulon definition, we deduced specific binding sites for FnrL, DnrD, DnrF and DnrE by comparing the promoter regions of the target genes. Furthermore, we created promoter-lacZ reporter gene fusions of target genes to analyse the anaerobic expression in more detail. FnrL was produced in E. coli and after purification we performed spectroscopic analysis.
Results
Global sequence alignments were performed and grouped FnrL of D. shibae DFL12T to a Roseobacter specific phylum of FnrN type regulators of Crp/ Fnr transcriptional regulators. UV/ Vis spectroscopy of the purified FnrL protein revealed binding of an oxygen sensitive Fe-S cluster which enables Fnr to measure oxygen tension and regulate anaerobic gene expression. DnrD, DnrF and DnrE were classified within the Dnr phylum of Crp/ Fnr regulators. In D. shibae DFL12T the denitrification genes were found clustered and transcribed in large transcriptional units. The napFDAGHBC operon, encoding the nitrate reduction step, is regulated in a close interplay of all four Crp/ Fnr regulators of D. shibae. The nirSECFDGHJN encoding the nitrite reductase and the norCBQDEF operon encoding nitric oxide reductase were transcribed divergently sharing an overlapping promoter region. Both operons were activated by FnrL in an oxygen dependent manner and by DnrD in response to nitric oxide. Using promoter-lacZ reporter gene fusions the regulation by FnrL and DnrD was analysed in detail. Based on the defined regulons of the analysed transcriptional regulators a hierarchical network for anaerobic regulation of gene expression in D. shibae was established.
Figure.: Regulation of the denitrification operons by FnrL, DnrD, DnrE and DnrF. (A) Heat map representation of denitrification gene expression patterns of mutant strains DS001(ΔfnrL), DS002(ΔdnrD), DS003(ΔdnrE) and DS004(ΔdnrF) compared to D. shibae DFL12T wild type strain grown under anaerobic conditions. The colored bars represent the expression level in log2 scale. Green indicates a relatively low expression level in the mutant strain which indicates activation by the regulator; red indicates relatively high expression levels in the mutant strain compared to the wild type indicating repression. (B) Denitrification operons with corresponding RNA sequencing data based transcriptional start sites and transcript quantification under aerobic (blue line) and anaerobic conditions (red line) of the wild type D. shibae DFL12T. Black horizontal arrows indicate open reading frames and the direction of transcription. Additionally, binding sites of FnrL, DnrD, DnrE and DnrF are indicated by flags. If the corresponding binding site was located within a promoter sequence, the corresponding distance to the transcriptional start was given. Green boxes indicate an activation by the given regulator, red boxes indicate a repression. Abbreviations: a1, apbE1; c1, cycA1; hyp, hypothetical gene; dD, dnrD; hA, hemA3; dE, dnrE
Regulatory network for the adaptation of Dinoroseobacter shibae to iron limitation
Objectives
The rhizobial iron regulator RirA from D. shibaebelongs to the Rrf2- family of transcription factors and is supposed to coordinate a Fe-S cluster and thereby measure iron availability [1].
Materials & Methods
A ∆rirA knockout mutant strain was created to analyze the role of the regulator in adaptation to iron limitation. To complement the ∆rirA mutant strain, a construct with a N-terminal StrepII-tag and a constitutive promoter was used. RirA protein fused with a StrepII-tag was recombinantly produced and purified under anaerobic conditions. UV/Vis and electron paramagnetic resonance (EPR) spectroscopy as well as whole cell Mössbauer analyses were used to determine the nature of the Fe-S cluster. The Fe content of the protein was determined with the atom absorbance spectroscopy (AAS). Four cysteine residues of RirA were changed to alanine via site directed mutagenesis of the corresponding gene. DNA binding of the anaerobically purified RirA wildtype was analyzed using electro mobility shift assays (EMSA).
Results
The ∆rirA mutant strain showed a reduced growth under iron limitation compared to the wild type strain indicating a role in iron-dependent gene regulation. Complementation of the ∆rirA mutant strain was successful since the complemented strain grew like the wild type strain. Analyses of anaerobically purified wildtype RirA using UV/Vis spectroscopy revealed an absorption shoulder at 420 nm, typical of Fe‑S cluster containing proteins. Using EPR and Mössbauer spectroscopy a [3Fe‑4S]1+ cluster was identified. AAS measurements of iron, resulting in a 3:1 ratio of iron per molecule RirA, supported [3Fe‑4S]1+ as cofactor. Since three of the four cysteine mutants of RirA showed a drastically reduced absorption in UV/Vis spectroscopy these cysteines may serve as ligands for [3Fe‑4S]1+ cluster. Using EMSA analyses, binding of RirA to hemB2 promoter sequences was shown.
Light-dependend regulation of photosynthesis-genes in Dinoroseobacter shibae
Objectives
Analyses of the role of Dshi_1135 in light-dependent regulation of Bchla biosynthesis in D. shibae.
Materials & Methods
We used in vivo UV/Vis spectroscopy to identify mutants with altered absorption spectra compared to the wild type strain. We defined the Dshi_1135 regulon by comparing transcript levels of the regulatory mutant strain with the D. shibae wild type strain grown in the dark. Furthermore, we created a bchF-lacZ reporter gene fusion to analyse the gene expression in more detail. The LOV-HisKA protein Dshi_1135 was recombinantly produced in E. coli and purified for biochemical analyses.
Results
Dshi_1135 encodes a protein consisting of a potential light-oxygen-voltage (LOV) domain fused to a histidine kinase domain. It shows 42 % identity to a blue light-activated HK from Erythrobacter litoralis from which structural data are available [3]. Inactivation of Dshi_1135 resulted in a complete loss of Bchla as shown by extraction and UV/Vis absorption measurement. Transcriptome analysis of the Dshi_1135 mutant strain compared to the wild type strain revealed loss of expression of the photosynthetic gene cluster. Additionally, in the D. shibae wild type strain DFL12T we found an increase of the bchF-lacZreporter gene fusion.
Methods/Activities
Publications
Ebert, M., Schweyen, P., Bröring, M., Laass, S., Härtig, E. & Jahn, D. (2017) Heme and nitric oxide binding by the transcriptional regulator DnrF from the marine bacterium Dinoroseobacter shibae increases napDpromoter affinity. J. Biol. Chem., in press
Ebert M, Laass S, Thürmer A, Roselius L, Eckweiler D, Daniel R, Härtig E, Jahn D (2017) FnrL and three Dnr regulators are used for the metabolic adaptation to low oxygen tension in Dinoroseobacter shibae. Frontiers in Microbiology 8:642
Patzelt D, Michael V, Päuker O, Ebert M, Tielen P, Jahn D, Tomasch J, Petersen J, Wagner-Döbler I (2016). Gene flow across genus barriers - conjugation of Dinoroseobacter shibae’s 191-kb killer plasmid into Phaeobacter inhibens and AHL-mediated expression of type IV secretion systems. Front Microbiol 7: 742 (DOI: 10.3389/fmicb.2016.00742).
Klingner A, Bartsch A, Dogs M, Wagner-Döbler I, Jahn D, Simon M, Brinkhoff T, Becker J, Wittmann C (2015) Large-scale 13C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose. Appl Environ Microbiol 81/7: 2408-2422.
Laass S, Kleist S, Bill N, Drueppell K, Kossmehl S, Woehlbrand L, Rabus R, Klein J, Rohde M, Bartsch A, Wittmann C, Schmidt-Hohagen K, Tielen P, Jahn D & Schomburg D (2014) Gene regulatory and metabolic adaptation processes of Dinoroseobacter shibae DFL12T during oxygen depletion, J Biol Chem., 289:13219-13231
Ebert M, Laaß S, Burghartz M, Petersen J, Koßmehl S, Wöhlbrand L, Rabus R, Wittmann C, Tielen P, Jahn D (2013) Transposon mutagenesis identified chromosomal and plasmid genes essential for adaptation of the marine bacterium Dinoroseobacter shibae to anaerobic conditions, J Bac 195: 4769-4777 (DOI: 10.1128/JB.00860-13).
Piekarski T, Jahn D & Tielen P (2011) Marine Mikrobiologie: Etablierung genetischer Werkzeuge für Bakterien der Roseobacter-Gruppe, BIOspektrum 04/11
Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G, Hahnke S, Han C, Jahn D, Kalhoefer D, Kiss H, Klenk HP, Kyrpides N, Liebl W, Liesegang H, Meincke L, Pati A, Petersen J, Piekarski T, Pommerenke C, Pradella S, Pukall R, Rabus R, Stackebrandt E, Thole S, Thompson L, Tielen P, Tomasch J, von Jan M, Wanphrut N, Wichels A, Zech H, Simon M (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J 4: 61-77 (DOI: 10.1038/ismej.2009.94).
Piekarski T, Buchholz I, Drepper T, Schobert M, Wagner-Doebler I, Tielen P & Jahn D (2009) Genetic tools for the investigation of Roseobacter clade bacteria, BMC Microbiology, 9: 265
Contribution to conferences
Ebert, M., Laaß, S., Eckweiler, D., Thürmer, A., Daniel, R., Härtig, E. and Jahn, D. 2017. FnrL and three Dnr regulators control the anaerobic adaptation in Dinoroseobacter shibae DFL12T. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Würzburg, Deutschland. Oral presentation
Becker, M., Heyber, S., Härtig, E., Jahn,D. 2017. The role of thelight-oxygen-voltage (LOV)-histidine kinase Dshi_1135 for regulationof the bacteriochlorophyllabiosynthesis in Dinoroseobacter shibae. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Würzburg, Deutschland. Poster.
Behringer, M., Härtig, E., Jahn,D. 2017. Identification of a [3Fe-4S]1+ cofactor and functional analysis of the iron responsive regulator RirA from Dinoroseobacter shibae. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Würzburg, Deutschland. Poster.
Ebert, M., Schweyen, P., Bröring, M., Härtig, E. and Jahn, D. 2016. Regulatory network for the adaptation to low oxygen tension of Dinoroseobacter shibae DFL12T. Tetrapyrolles, Chemistry & Biology of Gordon research conference (GRC): Biology of Heme, Chlorophyll, Porphyrins, Chlorins and Billins- The Pigments of Life, Newport, RI, USA. Poster.
Ebert, M., Härtig, E. and Jahn, D. 2016. Regulatory network of Dinoroseobacter shibae DFL12T for the adaptation to low oxygen tension. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Jena, Deutschland. Oral presentation.
Heyber, S., Härtig, E., Jahn,D. 2016. The regulation of the bacteriochlorophyll biosynthesis in Dinoroseobacter shibae. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Jena, Deutschland. Poster.
Behringer, M., Härtig, E., Jahn,D. 2016. Biochemical characterization and functional analysis of the iron responsive regulator RirA from Dinoroseobacter shibae. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Jena, Deutschland. Poster.
Ebert, M., Härtig, E. and Jahn, D. 2015. Regulation of anaerobic respiratory pathways in Dinoroseobacter shibae. Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Marburg, Deutschland. Poster.
Jacobs, J., Laaß, S., Heyber, S., Engelmann, S., Härtig, E., Jahn,D. 2015. Iron regulation in the marine microorganism Dinoroseobacter shibae, Jahrestagung der Vereinigung für Allgemeine und Angewandte Mikrobiologie (VAAM), Marburg, Deutschland. Poster.
Laaß, S., Klein, J., Heisig, M., Rohde, M., Tielen, P., Jahn, D. 2013. Regulation of anaerobic respiratory pathways in Dinoroseobacter shibae. VAAM, Bremen, Germany. Oral presentation.
Jacobs, J., Laaß, S., Tielen, P., Jahn, D. 2012. B5 Progress report and future perspectives. 7th Status Seminar of the Transregio 51, Hanse Wissenschaftskolleg, Delmenhorst, Germany. Oral presentation.
Laaß, S., Klein, J., Jahn, D., Tielen, P. 2012 Regulation of anaerobic respiratory pathways in Dinoroseobacter shibae. VAAM, Tübingen, Germany. Oral presentation.
Laaß, S., Klein, J., Heisig, M., Rohde, M., Tielen, P., Jahn, D. 2012. Regulation of anaerobic respiratory pathways in Dinoroseobacter shibae. Gordon Research Conference “Marine Microbes”. Lucca (Barga), Italy. Poster.
Laaß, S., Jacobs, J., Ebert, M., Heisig, M., Rhode, M., Tielen, P., Jahn, D. 2012. Regulation of anaerobic respiratory pathways in Dinoroseobacter shibae. 6th Status Seminar of the Transregio 51, HZI Braunschweig, Germany. Oral presentation.
Laaß, S., Klein, J., Jahn, D., Tielen, P., 2012. Anaerobic respiratory pathways in Dinoroseobacter shibae. Mibi Retreat, Burg Warberg, Helmstedt, Germany. Oral presentation.
Laaß, S., Ebert, M., Tüpker, R., Tielen, P., Jahn, D. 2011.Regulatory networks of the Dinoroseobacter shibae energy metabolism. 2th Status Seminar of the Transregio 51, HZI Braunschweig, Germany. Oral presentation.
Vacancies of TU Braunschweig
Career Service' Job Exchange
Merchandising
Term Dates
Courses
Degree Programmes
Information for Freshman
TUCard
Technische Universität Braunschweig
Universitätsplatz 2
38106 Braunschweig
P. O. Box: 38092 Braunschweig
GERMANY
Phone: +49 (0) 531 391-0